Molecular Plant Advance Access originally published online on July 30, 2009
Molecular Plant 2009 2(5):1015-1024; doi:10.1093/mp/ssp055
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Transcriptional Wiring of Cell Wall-Related Genes in Arabidopsis
Max-Planck-Institute for Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam, Germany
1 To whom correspondence should be addressed. E-mail Persson{at}mpimp-golm.mpg.de, fax +49-331-567-898149, tel. +49-331-567-8149.
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Abstract |
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Transcriptional coordination, or co-expression, of genes may signify functional relatedness of the corresponding proteins. For example, several genes involved in secondary cell wall cellulose biosynthesis are co-expressed with genes engaged in the synthesis of xylan, which is a major component of the secondary cell wall. To extend these types of analyses, we investigated the co-expression relationships of all Carbohydrate-Active enZYmes (CAZy)-related genes for Arabidopsis thaliana. Thus, the intention was to transcriptionally link different cell wall-related processes to each other, and also to other biological functions. To facilitate easy manual inspection, we have displayed these interactions as networks and matrices, and created a web-based interface (http://aranet.mpimp-golm.mpg.de/corecarb) containing downloadable files for all the transcriptional associations.
Key Words: Cell walls • bioinformatics • Arabidopsis • co-expression
Received for publication May 14, 2009. Accepted for publication July 3, 2009.
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INTRODUCTION |
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The past 10 years have seen an immense increase in publicly available biological information, including genome sequences, expression analyses, protein interaction data, and metabolite profiling (Schena et al., 1995; Li et al., 2004; Baerenfaller et al., 2008). A major challenge is to utilize, and integrate, the data to understand fundamental features of living organisms (Kitano, 2002). For example, Zhang et al. (2005) constructed a biological network for yeast based on five different types of interactions, including gene expression, protein interactions, and genetic interactions, and explored this network to identify common structures in the network that may explain the design principle for the network. Similar undertakings have not yet been attempted in plants, largely due to the lack of sufficient amounts of data. However, recently Hirai et al. (2007) integrated co-expression analysis and metabolite profiling to reveal novel components in secondary metabolism. Analogously, Geisler-Lee et al. (2007) produced a web-based predictive tool that uses co-expression and orthologous protein–protein interaction data from various species to predict novel, putative protein–protein interactions in Arabidopsis thaliana. While similar studies currently are emerging for plants, the most commonly used metric are microarray-based co-expression analyses (Aoki et al., 2007).
Co-expressed gene pairs may be functionally related (Stuart et al., 2003; Ihmels et al., 2004; Aoki et al., 2007 and references within). The relative success of this approach has resulted in several web-based co-expression tools, including CressExpress (Srinivasasainagendra et al., 2008), ATTED-II (Obayashi et al., 2009), ASIDB (Rawat et al., 2008), Genevestigator (Zimmermann et al., 2004), GeneCAT (Mutwil et al., 2008), CSB.DB (Steinhauser et al., 2004), and Expression Angler of the Bio-Array Resource (BAR; Toufighi et al., 2005). Perhaps the best explored co-expression relationships in Arabidopsis are the secondary cell wall cellulose synthase (CESA) genes (Persson et al., 2005; Brown et al., 2005). These studies used the three secondary wall CESA genes as baits to identify other genes that exhibited similar expression behaviors. Several of these genes encode proteins that are associated with the production of xylan, which is another major polymer of the secondary cell wall (Bauer et al., 2006; Peña et al., 2007; Persson et al., 2007a; Brown et al., 2007).
As indicated, both cellulose and xylan are components of the plant cell wall, which is largely composed of complex polysaccharides, and heavily glycosylated proteins, and determines the shape and structure of the plant body (Somerville et al., 2004). The polysaccharides are, with the exception of cellulose, synthesized in the Golgi apparatus, and assembled into larger structures after being delivered to the cell surface (Geisler et al., 2008). It is anticipated that the synthesis and modifications of different polymers are maintained in a coordinated fashion to assure an organized cell wall architecture (Geisler et al., 2008). While such coordination most likely is sustained by specific enzyme activity and selective vesicle shuttling, other cellular activities may also point towards synchronization of polymer formation. For example, several genes corresponding to enzymes involved in cellulose, xylan, and lignin production are transcriptionally coordinated (Persson et al., 2005; Brown et al., 2005). Similarly, Cocuron et al. (2007) showed that the synthesis of the glucan backbone in xyloglucan most likely is synthesized by a member of the cellulose synthase-like (CSL) family C, and that the corresponding gene was co-expressed with a xylosyltransferase also involved in xyloglucan synthesis. Co-expression analyses may therefore reveal functionally linked gene pairs, and also put biological processes in functional context to each other.
Enzymes that are linked to synthesis and modifications of cell wall polysaccharides, and glycan chains associated with cell wall proteins, can be found in the Carbohydrate-Active enZYmes (CAZy) database (www.cazy.org). CAZy holds information concerning sequences, putative biochemical activities, and classifications for carbohydrate-related enzymes from a range of different organisms (Cantarel et al., 2009). To explore potential functional relationships between carbohydrate-synthesizing proteins, we investigated the degree of co-expression of the corresponding genes, using CAZy as platform. We chose to focus on Arabidopsis in this study, as this model plant holds good gene predictions, and has produced abundant high-quality microarray data required for co-expression analysis.
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Division of CAZymes Based on Visual Inspection of Phylogenetic Trees
The CAZy database (www.cazy.org/) currently holds approximately 300 super-families divided into glycosyl hydrolases (GHs), glycosyl transferases (GTs), polysaccharide lyases (PLs), carbohydrate-binding modules (CBMs), and carbohydrate estrases (CEs; Cantarel et al., 2009). Any given protein is identified as belonging to a certain CAZy super-family based on sequence commonalities, and on its modular structure (Cantarel et al., 2009). While this approach provides a useful classification, it may also group enzymes that are synthesis-related, but produce different linkages that are associated with different polysaccharides. To increase the resolution of the individual super-families, we constructed phylogenetic trees containing all assigned Arabidopsis enzymes for each CAZy super-family, respectively. For example, the CAZy super-family GT2 contains 42 Arabidopsis proteins (Figure 1A). These enzymes are referred to as the Cellulose Synthase-like (CSL) super-family, and are believed to synthesize the backbones for cellulose and hemicelluloses, e.g. β-1,4-glucan linkages, during cell wall formation (Richmond, 2000). Several studies support the idea that certain sub-families of the GT2s are involved in the synthesis of different polymers. For example, while the 10 CESAs in Arabidopsis are believed to synthesize cellulose microfibrils (GT2-1s in Figure 1A; Arioli et al., 1998; Kimura et al., 1999; Paredez et al., 2006), the nine CSLAs (GT2-8s in Figure 1A) appear to synthesize the backbone of the hemicellulose mannan (Liepman et al., 2005; Dhugga et al., 2004). While the members of these two families produce structurally related linkages, these linkages may be part of different polysaccharides. We argued that the functional context, and therefore perhaps also the co-expressed context, for the gene products in these families may differ. To minimize functional overlaps of members in the CAZy super-families, we visually inspected each of the phylogenetic trees, and divided the super-families into putative families based on prominent clades (Figure 1A; http://aranet.mpimp-golm.mpg.de/corecarb). We subsequently used these families for the co-expression analyses.
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Transcriptional Associations between Different CAZy-Related Families in Arabidopsis
We explored the transcriptional associations between CAZy genes in Arabidopsis by using publicly available microarray data. Using the data, we constructed mutual rank-based correlation matrices for all the genes that corresponded to the CAZy proteins (Mutwil et al., 2008). We visualized connections below a certain mutual rank as networks, as such representations can display multiple gene associations, which is rather difficult to display in co-expression matrices. While various studies have used distinct Pearson r-value cut-offs to define significant levels of co-expression (e.g. van Noort et al., 2004), several recent reports have utilized mutual rank-based cut-offs (Mutwil et al., 2008; Obayashi et al., 2009). These values indicate whether the mutual co-expression rank of two genes is below a certain level. For example, if gene A is ranked as the seventh highest co-expressed gene with gene B, and gene B is the eleventh gene in the co-expression list for gene A, then their mutual rank corresponds to nine. Although this approach may exclude connections for genes that are well connected, it may also reveal biological information that is lost using a strict r-value cut-off. For example, several gene products have been indirectly connected to cellulose synthesis, including the GPI-anchored protein COBRA (COB; Roudier et al., 2005), and the chitinase-like protein POM1/CTL1 (Hauser et al., 1995; Mouille et al., 2003). However, a cut-off r-value of 0.8 did not associate these genes when using the primary CESA gene CESA6 as bait gene (r-values 0.77 and 0.75, respectively, using GeneCAT; Mutwil et al., 2008). On the contrary, using a mutual rank-based cut-off of 30 readily links the CESA6 gene with these genes (mutual ranks 4 and 9, respectively, using GeneCat; Mutwil et al., 2008). We chose a mutual rank cut-off of 30 to generate a co-expression network for all the genes associated with the different putative CAZy families, and then investigated whether certain families were connected more often than expected by chance (p
0.05). For example, if several genes in one CAZy family are co-expressed to several genes in another family, and if these relationships occur more frequently then expected by chance, we propose that genes belonging to these families are co-expressed. We estimated the relationships by sampling the co-expressed node (gene) vicinities for each individual gene (n = 2), namely nodes that are found within two steps from the bait gene, in the mutual rank-based network (Figure 1B; Mutwil et al., submitted elsewhere), and subsequently counted the co-occurrence of different CAZy family members. However, such relationships may become skewed if two or more genes from the same CAZy family are in the same co-expressed node vicinity. For instance, if two or more such genes are linked in a co-expression network, a large extent of the sampled area will be covered two times (Figure 1C). This is clear if we look at the CESA family in which CESA1, 2, 3, 5, and 6, and CESA4, 7, and 8 are in each other's node vicinities, respectively (Figure 1C). To avoid this type of skewed enrichment, we considered overlapping areas only once; in other words, if two of the genes from one family are within two steps’ distance from one another, we assign them to a regulon. For example, CESA1, 2, 3, 5, and 6 are all within two steps away from one another and were therefore assigned to one regulon (Figure 1D). The co-expression relationships between CAZy families, and between individual genes in these families, are available from http://aranet.mpimp-golm.mpg.de/corecarb.
Construction of a CAZy-Based Co-Expression Network
We depicted the co-expression relationships for the different CAZy families as a network structure, in which individual families represent nodes, and connections (edges) between the nodes represent significant co-expression (Figure 2A; http://aranet.mpimp.golm-mpg.de/corecarb). From this network, it is evident that, for example, the CESAs tend to be transcriptionally connected to members in family GT8-2 and in GT47-2 (Table 1 and Figure 2). The GT47 gene (At1g27440) that is co-expressed with the secondary CESA regulon corresponds to IRegular Xylem 10 (IRX10; Brown et al., 2007, 2009), and is necessary for the synthesis of xylan during secondary cell wall production. While the GT8-2 gene that is indicated as co-expressed with the secondary CESA regulon in Table 1 so far has not been reported to be involved in secondary cell wall synthesis, another GT8 gene that is associated with the GT8-1 family (IRX8; At5g54690) is also closely co-expressed with the secondary CESAs (Persson et al., 2005; Brown et al., 2005; http://aranet.mpimp-golm.mpg.de/aranet). It is currently hypothesized that the function of this gene is associated with initiation or capping of the polymer, or perhaps with cross-linking of the xylan polymer to other cell wall polymers (Peña et al., 2007; Persson et al., 2007a). The IRX10 gene product, on the other hand, appears to be associated with the elongation of the xylan backbone (Brown et al., 2009).
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Similarly, at least four GT8s from the same family (GT8-2) are present in close vicinity to the primary cell wall CESAs (Table 1). While xylan is not present to any larger extent in the primary cell wall, at least one of the GT8s has been shown to have galacturonosyltransferase activity (GAUT1; Sterling et al., 2006) presumably associated with the production of the pectic polymer homogalacturonan (HG). The GT8-2 family has been referred to as the GAUT-like clade (Sterling et al., 2006), and, if the four GT8-2s that are co-expressed with the primary wall CESAs also hold similar activities, it appears likely that they are involved in the synthesis of HG, which is prevalent during primary wall formation.
Associations of the Putative CAZy Families with Other Families (Pfams) in the Genome
While it may be useful to depict the transcriptional coordination between genes associated with the different CAZy families, it may also be of interest to explore the co-expression relationships between these genes and all the genes present on the ATH1 chip. Such analysis could reveal novel gene partners necessary for synthesis of specific polysaccharides. To do this, we took a similar approach as for detecting associations between the CAZy-based families. We grouped all genes present on the ATH1 chip into families according to the Pfam classification (Finn et al., 2008; http://pfam.sanger.ac.uk/). Similar to the CAZy family network, we used a mutual rank cut-off of 30, and considered all genes in the matrix that had a rank value below this value as co-expressed (http://aranet.mpimp.golm-mpg.de/corecarb). We subsequently analyzed whether genes of a certain Pfam co-occurred with genes of a certain CAZy family more than expected by chance (p 0.05). Based on these relationships, we created lists for each putative CAZy family, displaying the connections between the CAZy families and Arabidopsis Pfams (http://aranet.mpimp-golm.mpg.de/corecarb).
To illustrate the example above, we chose to focus on the co-expression between genes in the CESA family and different Pfam genes (Table 2). Interestingly, COBRA-related genes, which are not yet associated with any comprehensible biological function, are associated with three of the four CESA node regulons (Figure 1D and Table 2). COBRA1 is closely co-expressed with the primary wall CESAs, and results in reduced cellulose content and cell expansion deficiencies when mutated (Roudier et al., 2005). Analogously, the COBRA-like 4 gene is essential for secondary cell wall integrity, and is closely co-expressed with the secondary CESA genes (Brown et al., 2005). These two genes therefore appear to play essential roles during primary and secondary cell wall biosynthesis. In addition, COBRA-like 6 (COBL6; At1g09790) is co-expressed with CESA9 (Table 3), which is only expressed in mature pollen, and in seeds (data not shown). Considering that CESA9 appears to be functionally similar to another primary wall CESA, CESA6 (Persson et al., 2007b), the COBL6 may constitute an interesting candidate to further explore the functions of the COBRAs.
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Another interesting gene family that is transcriptionally connected to two of the four CESA node vicinities is the ‘multi-copper oxidase-related’ family (Table 2). Several such genes are co-expressed with the secondary wall-related CESAs, and are referred to as diphenol oxidases or laccases (Table 3). These include at least one gene that is essential for secondary cell wall deposition, IRX12 (At2g38080; Brown et al., 2005). At least five additional laccases are found in the close vicinity of the secondary wall CESAs, and are perhaps therefore likely to mask phenotypic traits in the absence of one of the other laccase-related genes. Another multi-copper-related gene is co-expressed with the primary wall CESAs (Table 3). This gene corresponds to SKU5 (At4g12420; Sedbrook et al., 2002), which encodes a glycosyl phosphatidylinositol-anchored glycoprotein that is involved in directional growth processes (Sedbrook et al., 2002). In addition, at least three SKU5-like genes, including SKS4 (At4g22010), SKS5 (At1g76160), and SKS6 (At1g41830) are in close vicinity to the primary CESA regulon (data not shown). These genes are closely related to each other, and the corresponding proteins may therefore be likely to perform similar functions, perhaps in concert with SKU5.
Some other Pfams that may be interesting to investigate are the ‘Protein kinase domain’ and ‘Protein tyrosine kinase’ families (Table 3). A multitude of such genes are co-regulated with the primary wall CESA regulon (Table 3). While most of these are Receptor-like kinases (RLKs) of unknown function, several of them have been associated with cell elongation. For example, THESEUS1 (THE1; At5g54380), which suppresses the mutant phenotype prc1-1 (affecting the primary CESA, CESA6) when mutated, has recently been suggested to be involved in sensing primary cell wall integrity (Hématy et al., 2007). In addition, another RLK FEI1 (At1g31420; Xu et al., 2008) is necessary for primary wall deposition and for root elongation, and is also co-expressed with the primary CESAs (Table 3). Several of the other RLKs associated with the primary CESA regulon may therefore be relevant targets for further insight into cell wall signaling. Furthermore, multiple genes with the same Pfams are also co-expressed with the secondary CESA regulon, and may perhaps therefore be associated with regulation of secondary wall polymer synthesis.
In summary, we have investigated co-expression relationships for the different CAZy families. This approach exposes both gene correlations on an individual gene level, and also provides insight into how multiple members of the different families are transcriptionally linked. In addition, we extended the analyses to include all genes on the ATH1 chip, and explored co-expression relationships between the different CAZy families and Pfams. All of the results are downloadable from http://aranet.mpimp-golm.mpg.de/corecarb as text, and excel files. Co-expression networks for individual genes can be mined at http://aranet.mpimp-golm.mpg.de/aranet (Mutwil et al., submitted elsewhere).
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Microarray Data
All calculations for this work were done using python and java code. The datasets are the same as used for the GeneCAT webtool (Mutwil et al. 2008). Specifically, databases for Arabidopsis use Affymetrix ATH1 (22 810 probe sets) Arabidopsis microarray datasets consisting of 1428 ATH1 microarrays, which were obtained from TAIR (www.Arabidopsis.org/). The microarray data were quality controlled by visual inspection of boxplots of raw PM data and RMA residuals of RMA normalized data, using the RMA express program. Cel files showing artifacts on RMA residual plots or visibly deviating from the majority on the PM-boxplots were removed from further analysis. In addition, we removed experiments representing very similar transcriptomic snapshots by iteratively discarding microarrays that displayed Pearson correlation r(A,B)
0.95 to more than three other microarrays. From these analyses, we retained 351 microarrays, which subsequently were normalized using R package simpleAffy.
Phylogenetic Analysis of CAZy Families
Arabidopsis thaliana gene identifiers (AGI codes) for the different carbohydrate active enzymes super-families were downloaded from the CAZy database (www.cazy.com). The protein sequences of the super-families were then aligned by clustalW in the MEGA software package using standard settings (Tamura et al., 2007). The resulting alignments were then subjected to Neighbor Joining algorithm, exported as phylogenetic trees, and clades were extracted. We chose to divide the trees by visual inspection, as neither tree branch length nor BLAST score cut-off values can reliably identify groups of similar genes.
Division of Arabidopsis thaliana Proteins into Families using PFAM
Each probeset in the Affymetrix ATH1 microarray platform was mapped using BLAST (Altschul et al., 1990) to the corresponding best-hit coding sequence as defined by TAIR8 (www.Arabidopsis.org/). Probesets with no gene hit or expected values higher than 0.01 were excluded from further analysis.
Using reversed position-specific BLAST (RPS-BLAST; Marchler-Bauer et al., 2002) with a cut-off expected value of 0.01, we assigned each Arabidopsis gene to the best-hit Pfam family (Finn et al., 2008, Pfam v23.0).
Calculating Statistical Significance of Family Associations
To obtain empirical p-values for the co-association of the different families, the family tags were shuffled 10 000 times. During each shuffling, the number of instances in which any two proteins could be found in each other's network vicinity (n = 2) was counted, and the number was divided by 10 000 to obtain the p-value. The co-expressed network vicinity was generated by moving two steps out from a node of interest; thus, any gene that is a direct neighbor or a neighbor of a neighbor is included in the node vicinity. Any two families associated with a p-value < 0.05 were called ‘p-value co-regulated’.
To obtain the number of protein families present in separate regulons of each family, members of a family were recursively grouped together if they were neighbors in a co-expression network (i.e. within two steps away from each other). The obtained regulons were then examined for presence of protein families. If any protein family was found in two or more regulons, it was called ‘regulon co-regulated’. Finally, any two families were called significantly co-regulated if they were both p-value and regulon co-regulated.
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This work was funded by the Max-Planck-Gesellschaft.
No conflict of interest declared.
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